The biological functions of the epitranscriptomic modification N 6 -methyladenosine (m 6 A) in plants are not fully understood. CPSF30-L is a predominant isoform of the polyadenylation factor CPSF30 and consists of CPSF30-S and an m 6 A-binding YTH domain. Little is known about the biological roles of CPSF30-L and the molecular mechanism underlying its m 6 A-binding function in alternative polyadenylation. Here, we characterized CPSF30-L as an Arabidopsis m 6 A reader whose m 6 A-binding function is required for the floral transition and abscisic acid (ABA) response. We found that the m 6 A-binding activity of CPSF30-L enhances the formation of liquid-like nuclear bodies, where CPSF30-L mainly recognizes m 6 A-modified far-upstream elements to control polyadenylation site choice. Deficiency of CPSF30-L lengthens the 3 0 untranslated region of three phenotypes-related transcripts, thereby accelerating their mRNA degradation and leading to late flowering and ABA hypersensitivity. Collectively, this study uncovers a new molecular mechanism for m 6 A-driven phase separation and polyadenylation in plants.

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Background N6-methyladenosine (m6A) mRNA modification is essential for mammalian and plant viability. The U6 m6A methyltransferases in other species regulate S-adenosylmethionine (SAM) homeostasis through installing m6A in pre-mRNAs of SAM synthetases. However, U6 m6A methyltransferase has not been characterized in Arabidopsis and little is known about its role in regulating photomorphogenesis and flowering. Results Here we characterize that FIONA1 is an Arabidopsis U6 m6A methyltransferase that installs m6A in U6 snRNA and a small subset of poly(A)+ RNA. Disruption of FIONA1 leads to phytochrome signaling-dependent hypocotyl elongation and photoperiod-independent early flowering. Distinct from mammalian METTL16 and worm METT-10, FIONA1 neither installs m6A in the mRNAs of Arabidopsis SAM synthetases nor affects their transcript expression levels under normal or high SAM conditions. We confirm that FIONA1 can methylate plant mRNA m6A motifs in vitro and in vivo. We further show that FIONA1 installs m6A in several phenotypic related transcripts, thereby affecting downstream mRNA stability and regulating phytochrome signaling and floral transition. Conclusion FIONA1 is functional as a U6 m6A methyltransferase in Arabidopsis, distinct from mammalian METTL16 and worm METT-10. Our results demonstrate that FIONA1-mediated m6A post-transcriptional regulation is an autonomous regulator for flowering and phytochrome signaling-dependent photomorphogenesis.